Achievements and open questions in the self-reproduction of vesicles and synthetic minimal cells.

Supramolecular chemistry was enriched, about twenty years ago, by the discovery of the self-reproduction of micelles and vesicles. The dynamic aspects and complexity of these systems makes them good models for biological compartments. For example, the self-reproduction of vesicles suggests that the growth in size and number of a vesicle population resembles the pattern of living cells in several aspects, but it take place solely due to physical forces. Several reports demonstrate that reverse micelles, micelles, sub-micrometric and giant vesicles can self-reproduce, generating new particles at the expenses of a suitable precursor. Recently, similar studies are in progress on more complex vesicle-based systems, namely semi-synthetic minimal cells. These are artificial cell-like compartments that are built by filling liposomes with the minimal number of biomolecules, such as DNA, ribosomes, enzymes, etc., in order to construct a living cell in the laboratory. This approach aims to investigate the minimal requirements for molecular systems in order to display some living properties, while it finds relevance in origins of life studies and in synthetic (constructive) biology.

[1]  P. Walde Surfactant Assemblies and their Various Possible Roles for the Origin(S) of Life , 2006, Origins of Life and Evolution of Biospheres.

[2]  Pasquale Stano,et al.  From Never Born Proteins to Minimal Living Cells: Two Projects in Synthetic Biology , 2007, Origins of Life and Evolution of Biospheres.

[3]  P. Luisi,et al.  Autopoiesis with or without cognition: defining life at its edge , 2004, Journal of The Royal Society Interface.

[4]  A. Rushdi,et al.  Lipid Formation by Aqueous Fischer-Tropsch-Type Synthesis over a Temperature Range of 100 to 400 °C , 2001, Origins of life and evolution of the biosphere.

[5]  M. Hicks,et al.  Ufasomes are Stable Particles surrounded by Unsaturated Fatty Acid Membranes , 1973, Nature.

[6]  Pasquale Stano,et al.  Lecithin‐Based Water‐In‐Oil Compartments as Dividing Bioreactors , 2007, Chembiochem : a European journal of chemical biology.

[7]  J. Szostak,et al.  Template-directed synthesis of a genetic polymer in a model protocell , 2008, Nature.

[8]  B. Simoneit,et al.  Lipid Synthesis Under Hydrothermal Conditions by Fischer- Tropsch-Type Reactions , 1999, Origins of life and evolution of the biosphere.

[9]  David W. Deamer,et al.  Stability of Model Membranes in Extreme Environments , 2008, Origins of Life and Evolution of Biospheres.

[10]  P. Luisi,et al.  Lipase-catalyzed reactions in vesicles as an approach to vesicle self-reproduction. , 1994, Journal of liposome research.

[11]  P. Luisi,et al.  Self-Reproduction of Micelles and Liposomes and the Transition to Life , 1993 .

[12]  T. Buhse,et al.  Phase-Transfer Model for the Dynamics of ``Micellar Autocatalysis'' , 1997 .

[13]  Pasquale Stano,et al.  Approaches to semi-synthetic minimal cells: a review , 2005, Naturwissenschaften.

[14]  P. Luisi,et al.  Enzymatic RNA replication in self-reproducing vesicles: an approach to a minimal cell. , 1995, Biochemical and biophysical research communications.

[15]  Ricard V Solé,et al.  Evolution and self-assembly of protocells. , 2009, The international journal of biochemistry & cell biology.

[16]  T. Haines Anionic lipid headgroups as a proton-conducting pathway along the surface of membranes: a hypothesis. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[17]  J. Wattis,et al.  Size-Templating Matrix Effect in Vesicle Formation. 2. Analysis of a Macroscopic Model , 2003 .

[18]  Taro Toyota,et al.  A novel system of self-reproducing giant vesicles. , 2003, Journal of the American Chemical Society.

[19]  Takuya Ueda,et al.  Cell-free translation reconstituted with purified components , 2001, Nature Biotechnology.

[20]  Pier Luigi Luisi,et al.  Insights into the self-reproduction of oleate vesicles , 2006 .

[21]  Irene A Chen,et al.  A kinetic study of the growth of fatty acid vesicles. , 2004, Biophysical journal.

[22]  P. Walde,et al.  Fatty acid vesicles , 2007 .

[23]  P. Luisi,et al.  The Use of Liposomes for Constructing Cell Models , 2002, Journal of biological physics.

[24]  Pier Luigi Luisi,et al.  The Notion of a DNA Minimal Cell: A General Discourse and Some Guidelines for an Experimental Approach , 2002 .

[25]  Peter V. Coveney,et al.  Becker–Döring model of self-reproducing vesicles , 1998 .

[26]  Yutetsu Kuruma Question 7: Biosynthesis of Phosphatidic Acid in Liposome Compartments – Toward the Self-Reproduction of Minimal Cells , 2007, Origins of Life and Evolution of Biospheres.

[27]  K. Yoshikawa,et al.  Spontaneous Formation of Giant Liposomes from Neutral Phospholipids , 1997 .

[28]  Pier Luigi Luisi,et al.  Enzymatic RNA Synthesis in Self-Reproducing Vesicles: An Approach to the Construction of a Minimal Synthetic Cell , 1994 .

[29]  Fabio Mavelli,et al.  Cooperative Micelle Binding and Matrix Effect in Oleate Vesicle Formation , 2003 .

[30]  D. Lasič On the thermodynamic stability of liposomes , 1990 .

[31]  David W. Deamer,et al.  Boundary structures are formed by organic components of the Murchison carbonaceous chondrite , 1985, Nature.

[32]  P. Coveney,et al.  Kinetics of self-replicating micelles , 1994 .

[33]  L. Mandell,et al.  Phase equilibria and phase structure in the ternary systems sodium or potassium octanoate-octanoic acid-water , 1993 .

[34]  Martin Nilsson,et al.  Bridging Nonliving and Living Matter , 2003, Artificial Life.

[35]  G. Murtas,et al.  Internal lipid synthesis and vesicle growth as a step toward self-reproduction of the minimal cell , 2009, Systems and Synthetic Biology.

[36]  G. von Kiedrowski,et al.  Systems chemistry: kinetic and computational analysis of a nearly exponential organic replicator. , 2005, Angewandte Chemie.

[37]  Monpichar Srisa-Art,et al.  Microdroplets: a sea of applications? , 2008, Lab on a chip.

[38]  Steen Rasmussen,et al.  Nucleobase mediated, photocatalytic vesicle formation from an ester precursor. , 2009, Journal of the American Chemical Society.

[39]  Pier Luigi Luisi,et al.  Autocatalytic self-replicating micelles as models for prebiotic structures , 1992, Nature.

[40]  N. Packard,et al.  Transitions from Nonliving to Living Matter , 2004, Science.

[41]  P. Luisi,et al.  Toward the engineering of minimal living cells , 2002, The Anatomical record.

[42]  P. Walde,et al.  Kinetic studies of the interaction of fatty acids with phosphatidylcholine vesicles (liposomes). , 2006, Colloids and surfaces. B, Biointerfaces.

[43]  T. Sugawara,et al.  Membrane dynamics of a myelin-like giant multilamellar vesicle applicable to a self-reproducing system. , 2004, Langmuir : the ACS journal of surfaces and colloids.

[44]  P. Luisi,et al.  Light microscopic investigations of the autocatalytic self-reproduction of giant vesicles , 1995 .

[45]  Alberto Diaspro,et al.  Protein synthesis in liposomes with a minimal set of enzymes. , 2007, Biochemical and biophysical research communications.

[46]  S. Svetina,et al.  Vesicle self-reproduction: The involvement of membrane hydraulic and solute permeabilities , 2007, The European physical journal. E, Soft matter.

[47]  S. Svetina,et al.  Growth and shape transformations of giant phospholipid vesicles upon interaction with an aqueous oleic acid suspension. , 2009, Chemistry and physics of lipids.

[48]  P. Luisi,et al.  Autopoietic Self-Reproduction of Fatty Acid Vesicles , 1994 .

[49]  P. Luisi,et al.  Novel properties of DDAB: Matrix effect and interaction with oleate , 2004 .

[50]  Pasquale Stano,et al.  Synthetic biology of minimal living cells: primitive cell models and semi-synthetic cells , 2010, Systems and Synthetic Biology.

[51]  D. Zakim,et al.  Fatty acid flip-flop in phospholipid bilayers is extremely fast. , 1995, Biochemistry.

[52]  Pasquale Stano,et al.  Chemical approaches to synthetic biology. , 2009, Current opinion in biotechnology.

[53]  Pier Luigi Luisi,et al.  Coexistence and Mutual Competition of Vesicles with Different Size Distributions , 2003 .

[54]  Roberto Serra,et al.  Synchronization Phenomena in Surface-Reaction Models of Protocells , 2007, Artificial Life.

[55]  D. Cistola,et al.  Ionization and phase behavior of fatty acids in water: application of the Gibbs phase rule. , 1988, Biochemistry.

[56]  M. Ueno,et al.  Effect of preformed egg phosphatidylcholine vesicles on spontaneous vesiculation of oleate micelles , 2005 .

[57]  D. Deamer,et al.  Chemical evolution of amphiphiles: glycerol monoacyl derivatives stabilize plausible prebiotic membranes. , 2009, Astrobiology.

[58]  H. Itoh,et al.  Preparation of giant liposomes in physiological conditions and their characterization under an optical microscope. , 1996, Biophysical journal.

[59]  Martin M Hanczyc,et al.  Replicating vesicles as models of primitive cell growth and division. , 2004, Current opinion in chemical biology.

[60]  Vincent Noireaux,et al.  A vesicle bioreactor as a step toward an artificial cell assembly. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[61]  Javier Macía,et al.  Protocell self-reproduction in a spatially extended metabolism-vesicle system. , 2005, Journal of theoretical biology.

[62]  P. Walde,et al.  Thermodynamic and kinetic stability. Properties of micelles and vesicles formed by the decanoic acid/decanoate system , 2003 .

[63]  H. Hauser,et al.  Kinetics and mechanism of long-chain fatty acid transport into phosphatidylcholine vesicles from various donor systems. , 2002, Biochemistry.

[64]  Pier Luigi Luisi,et al.  Liposome-mediated enzymatic synthesis of phosphatidylcholine as an approach to self-replicating liposomes , 1991 .

[65]  B. Ninham,et al.  Theory of self-assembly of lipid bilayers and vesicles. , 1977, Biochimica et biophysica acta.

[66]  Pasquale Stano,et al.  Vesicle behavior: in search of explanations. , 2008, The journal of physical chemistry. B.

[67]  Pasquale Stano,et al.  The Minimal Size of Liposome‐Based Model Cells Brings about a Remarkably Enhanced Entrapment and Protein Synthesis , 2009, Chembiochem : a European journal of chemical biology.

[68]  D. Deamer,et al.  Chemistry and Physics of Primitive Membranes , 2006 .

[69]  D. Lasic Spontaneous Vesiculation and Spontaneous Liposomes , 1999 .

[70]  Fabio Mavelli,et al.  Matrix Effect in Oleate Micelles-Vesicles Transformation , 2004, Origins of life and evolution of the biosphere.

[71]  D. Bartel,et al.  Synthesizing life : Paths to unforeseeable science & technology , 2001 .

[72]  K. Kaneko,et al.  Population study of sizes and components of self-reproducing giant multilamellar vesicles. , 2008, Langmuir : the ACS journal of surfaces and colloids.

[73]  Pier Luigi Luisi,et al.  Self-replicating Reverse Micelles and Chemical Autopoiesis , 1990 .

[74]  F. Kamp,et al.  pH gradients across phospholipid membranes caused by fast flip-flop of un-ionized fatty acids. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[75]  Pier Luigi Luisi,et al.  Matrix Effect of Vesicle Formation As Investigated by Cryotransmission Electron Microscopy , 2001 .

[76]  Antonio Lazcano,et al.  Comparative Genomics and the Gene Complement of a Minimal Cell , 2004, Origins of life and evolution of the biosphere.

[77]  P. Luisi,et al.  Lipid vesicles as possible intermediates in the origin of life , 1999 .

[78]  Yutetsu Kuruma,et al.  A synthetic biology approach to the construction of membrane proteins in semi-synthetic minimal cells. , 2009, Biochimica et biophysica acta.

[79]  D. Deamer,et al.  Liposomes from ionic, single-chain amphiphiles. , 1978, Biochemistry.

[80]  D. Deamer,et al.  Synthesis of phospholipids and membranes in prebiotic conditions , 1977, Nature.

[81]  Are Micelles and Vesicles Chemical Equilibrium Systems , 2001 .

[82]  Tetsuya Yomo,et al.  Femtoliter compartment in liposomes for in vitro selection of proteins. , 2006, Analytical biochemistry.

[83]  Tetsuya Yomo,et al.  Expression of a cascading genetic network within liposomes , 2004, FEBS letters.

[84]  Dan S. Tawfik,et al.  Man-made cell-like compartments for molecular evolution , 1998, Nature Biotechnology.

[85]  P. Luisi,et al.  Polymerase chain reaction in liposomes. , 1995, Chemistry & biology.

[86]  M. Ueno,et al.  Size control of mixed egg yolk phosphatidylcholine (EggPC)/oleate vesicles. , 2004, Chemical & pharmaceutical bulletin.

[87]  F. Mavelli,et al.  Stochastic simulations of minimal self-reproducing cellular systems , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[88]  Fabio Mavelli,et al.  Autopoietic Self-Reproducing Vesicles: A Simplified Kinetic Model , 1996 .

[89]  S. Svetina,et al.  A relationship between membrane properties forms the basis of a selectivity mechanism for vesicle self-reproduction , 2004, European Biophysics Journal.

[90]  M. Ueno,et al.  New vesicle formation upon oleate addition to preformed vesicles. , 2005, Chemical & pharmaceutical bulletin.

[91]  J. Lawless,et al.  Quantification of monocarboxylic acids in the Murchison carbonaceous meteorite , 1979, Nature.

[92]  Kazufumi Hosoda,et al.  Replication of Genetic Information with Self‐Encoded Replicase in Liposomes , 2008, ChemBioChem.

[93]  Pier Luigi Luisi,et al.  Chemical Aspects of Synthetic Biology , 2007, Chemistry & biodiversity.

[94]  P. Luisi The Emergence of Life: Autopoiesis: the logic of cellular life , 2006 .

[95]  Steen Rasmussen,et al.  Metabolic Photofragmentation Kinetics for a Minimal Protocell: Rate-Limiting Factors, Efficiency, and Implications for Evolution , 2008, Artificial Life.

[96]  Benjamin G Davis,et al.  Sugar synthesis in a protocellular model leads to a cell signalling response in bacteria. , 2009, Nature chemistry.

[97]  P. Walde,et al.  An Electron Spin Resonance Study of the pH-Induced Transformation of Micelles to Vesicles in an Aqueous Oleic Acid/Oleate System , 2001 .

[98]  Johanna Stankiewicz,et al.  Chembiogenesis 2005 and Systems Chemistry Workshop , 2006 .

[99]  Duccio Fanelli,et al.  Thermodynamics of vesicle growth and instability. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[100]  Pier Luigi Luisi,et al.  Growth and Transformation of Vesicles Studied by Ferritin Labeling and Cryotransmission Electron Microscopy , 2001 .

[101]  Pier Luigi Luisi,et al.  Matrix Effect in the Size Distribution of Fatty Acid Vesicles , 1998 .

[102]  P. Walde,et al.  An ESR characterization of micelles and vesicles formed in aqueous decanoic acid/sodium decanoate systems using different spin labels. , 2008, Chemistry and physics of lipids.

[103]  P. Luisi Autopoiesis: a review and a reappraisal , 2003, Naturwissenschaften.

[104]  Pier Luigi Luisi,et al.  A Matrix Effect in Mixed Phospholipid/Fatty Acid Vesicle Formation , 1999 .

[105]  D. Deamer,et al.  Role of lipids in prebiotic structures. , 1980, Bio Systems.

[106]  Naoaki Ono,et al.  Computational studies on conditions of the emergence of autopoietic protocells. , 2005, Bio Systems.

[107]  Kenichi Yoshikawa,et al.  Gene Expression within Cell‐Sized Lipid Vesicles , 2003, ChemBioChem.

[108]  Ricard V. Solé,et al.  Life Cycle of a Minimal ProtocellA Dissipative Particle Dynamics Study , 2007, Artificial Life.

[109]  Jonathan A. D. Wattis,et al.  The Size-Templating Matrix Effect in Vesicle Formation I: A Microscopic Model and Analysis , 2003 .

[110]  J. Szostak,et al.  Coupled Growth and Division of Model Protocell Membranes , 2009, Journal of the American Chemical Society.

[111]  Pierre-Alain Monnard,et al.  Models of primitive cellular life: polymerases and templates in liposomes , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[112]  Pier Luigi Luisi,et al.  Self-replicating micelles: aqueous micelles and enzymatically driven reactions in reverse micelles , 1991 .

[113]  Pier Luigi Luisi,et al.  OPARIN'S REACTIONS REVISITED : ENZYMATIC SYNTHESIS OF POLY(ADENYLIC ACID) IN MICELLES AND SELF-REPRODUCING VESICLES , 1994 .

[114]  M Wakabayashi,et al.  Synthesis of functional protein in liposome. , 2001, Journal of bioscience and bioengineering.

[115]  Kenichi Yoshikawa,et al.  Giant Liposome as a Biochemical Reactor: Transcription of DNA and Transportation by Laser Tweezers , 2001 .

[116]  F. Menger,et al.  Chemically-induced birthing and foraging in vesicle systems , 1994 .

[117]  Fabio Mavelli,et al.  A Possible Route to Prebiotic Vesicle Reproduction , 2004, Artificial Life.

[118]  T. Buhse,et al.  Origin of Autocatalysis in the Biphasic Alkaline Hydrolysis of C-4 to C-8 Ethyl Alkanoates , 1998 .

[119]  F. Varela,et al.  Self-replicating micelles — A chemical version of a minimal autopoietic system , 1989, Origins of life and evolution of the biosphere.

[120]  P. Luisi,et al.  Protein expression in liposomes. , 1999, Biochemical and biophysical research communications.

[121]  Ronald R. Breaker,et al.  Production of RNA by a polymerase protein encapsulated within phospholipid vesicles , 1994, Journal of Molecular Evolution.